The circadian clock is regulated by signaling networks that enhance a plant's ability to coordinate internal events with the external environment. In this study, we examine the rhythmic expression of long non-coding RNAs (lncRNAs) using multiple transcriptomes of Arabidopsis thaliana in the diel light cycle and integrated this information to have a better understanding of the functions of lncRNAs in regulating the circadian clock. We identified 968, 1050, and 998 lncRNAs at 8 h light, 16 h light and 8 h dark conditions, respectively. Among these, 423, 486, and 417 lncRNAs were uniquely present at 8 h light, 16 h light, and 8 h dark, respectively, whereas 334 lncRNAs were common under the three conditions. The specificity of identified lncRNAs under different light conditions was verified using qRT-PCR. The identified lncRNAs were less GC-rich and expressed at a significantly lower level than the mRNAs of protein-coding genes. In addition, we identified enriched motifs in lncRNA transcribing regions that were associated with light-responsive genes (SORLREP and SORLIP), flower development (AGAMOUS), and circadian clock (CCA1) under all three light conditions. We identified 10 and 12 different lncRNAs targeting different miRNAs with perfect and interrupted complementarity (endogenous target mimic). These predicted lncRNA-interacting miRNAs govern the function of a set of genes involved in the developmental process, reproductive structure development, gene silencing and transcription regulation. We demonstrated that the lncRNA transcribing regions were enriched for epigenetic marks such as H3.3, H3K4me2, H3K4me3, H4K16ac, H3K36ac, H3K56ac and depleted for heterochromatic (H3K9me2 and H3K27me1) and repressive (H3K27me3) histone modifications. Further, we found that hypermethylated genomic regions negatively correlated with lncRNA transcribing regions. Overall, our study showed that lncRNAs expressed corresponding to the diel light cycle are implicated in regulating the circadian rhythm and governing the developmental stage-specific growth.
